Promoter nucleosome dynamics regulated by signaling through the CTD code

  1. Philippe Materne
  2. Jayamani Anandhakumar
  3. Valerie Migeot
  4. Ignacio Soriano
  5. Carlo Yague-Sanz
  6. Elena Hidalgo
  7. Carole Mignion
  8. Luis Quintales
  9. Francisco Antequera
  10. Damien Hermand  Is a corresponding author
  1. University of Namur, Belgium
  2. LSU Health Sciences Center, United States
  3. Universidad de Salamanca, Spain
  4. Universitat Pompeu Fabra, Spain

Abstract

The phosphorylation of the RNA polymerase II CTD plays a key role in delineating transcribed regions within chromatin by recruiting histone methylases and deacetylases. Using genome-wide nucleosome mapping, we show that CTD S2 phosphorylation controls nucleosome dynamics in the promoter of a subset of 324 genes, including the regulators of cell differentiation ste11 and metabolic adaptation inv1. Mechanistic studies on these genes indicate that during gene activation a local increase of phosphoS2 CTD nearby the promoter impairs the phosphoS5 CTD dependent recruitment of Set1 and the subsequent recruitment of specific HDACs, which leads to nucleosome depletion and efficient transcription. The early increase of phosphoS2 results from the phosphorylation of the CTD S2 kinase Lsk1 by MAP kinase in response to cellular signaling. The artificial tethering of the Lsk1 kinase at the ste11 promoter is sufficient to activate transcription. Therefore, signaling through the CTD code regulates promoter nucleosomes dynamics.

Article and author information

Author details

  1. Philippe Materne

    Namur Research College, University of Namur, Namur, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  2. Jayamani Anandhakumar

    Department of Biochemistry and Molecular Biology, LSU Health Sciences Center, Shreveport, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Valerie Migeot

    Namur Research College, University of Namur, Namur, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  4. Ignacio Soriano

    Instituto de Biología Funcional y Genómica, Consejo Superior de Investigaciones Científicas, Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Carlo Yague-Sanz

    Namur Research College, University of Namur, Namur, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  6. Elena Hidalgo

    Departament de Ciencies Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Carole Mignion

    Namur Research College, University of Namur, Namur, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  8. Luis Quintales

    Instituto de Biología Funcional y Genómica, Consejo Superior de Investigaciones Científicas, Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Francisco Antequera

    Instituto de Biología Funcional y Genómica, Consejo Superior de Investigaciones Científicas, Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  10. Damien Hermand

    Namur Research College, University of Namur, Namur, Belgium
    For correspondence
    Damien.Hermand@unamur.be
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Danny Reinberg, Howard Hughes Medical Institute, New York University School of Medicine, United States

Version history

  1. Received: May 26, 2015
  2. Accepted: June 19, 2015
  3. Accepted Manuscript published: June 22, 2015 (version 1)
  4. Version of Record published: July 15, 2015 (version 2)

Copyright

© 2015, Materne et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Philippe Materne
  2. Jayamani Anandhakumar
  3. Valerie Migeot
  4. Ignacio Soriano
  5. Carlo Yague-Sanz
  6. Elena Hidalgo
  7. Carole Mignion
  8. Luis Quintales
  9. Francisco Antequera
  10. Damien Hermand
(2015)
Promoter nucleosome dynamics regulated by signaling through the CTD code
eLife 4:e09008.
https://doi.org/10.7554/eLife.09008

Share this article

https://doi.org/10.7554/eLife.09008

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